Differential responses of Bradyrhizobium sp. SUTN9-2 to plant extracts and implications for endophytic interactions within different host plants

Abstract Bradyrhizobium sp. strain SUTN9-2 demonstrates cell enlargement, increased DNA content, and efficient nitrogen fixation in response to rice (Oryza sativa) extract. This response is attributed to the interaction between the plant’s cationic antimicrobial peptides (CAMPs) and the Bradyrhizobi...

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Main Authors: Teerana Greetatorn, Pakpoom Boonchuen, Pongdet Piromyou, Pongpan Songwattana, Jenjira Wongdee, Kamonluck Teamtisong, Nantakorn Boonkerd, Shusei Sato, Neung Teaumroong, Panlada Tittabutr
Format: Article
Language:English
Published: Nature Portfolio 2025-01-01
Series:Scientific Reports
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Online Access:https://doi.org/10.1038/s41598-025-87488-5
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author Teerana Greetatorn
Pakpoom Boonchuen
Pongdet Piromyou
Pongpan Songwattana
Jenjira Wongdee
Kamonluck Teamtisong
Nantakorn Boonkerd
Shusei Sato
Neung Teaumroong
Panlada Tittabutr
author_facet Teerana Greetatorn
Pakpoom Boonchuen
Pongdet Piromyou
Pongpan Songwattana
Jenjira Wongdee
Kamonluck Teamtisong
Nantakorn Boonkerd
Shusei Sato
Neung Teaumroong
Panlada Tittabutr
author_sort Teerana Greetatorn
collection DOAJ
description Abstract Bradyrhizobium sp. strain SUTN9-2 demonstrates cell enlargement, increased DNA content, and efficient nitrogen fixation in response to rice (Oryza sativa) extract. This response is attributed to the interaction between the plant’s cationic antimicrobial peptides (CAMPs) and the Bradyrhizobium BacA-like transporter (BclA), similar to bacteroid in legume nodules. The present study reveals that SUTN9-2 can also establish functional endophytic interactions with chili (Capsicum annuum) and tomato (Solanum lycopersicum) plants. When exposed to extracts from chili and tomato, SUTN9-2 exhibits cell elongation, polyploidy, and reduced cell viability, with the effects being less pronounced for tomato extract. Transcriptomic and cytological analyses revealed that genes associated with CAMP resistance, nitrogen metabolism, nitrogen fixation, defense responses, and secretion systems were upregulated, while genes related to the cell cycle and certain CAMP-resistance mechanisms were downregulated, particularly in response to chili extract. This study suggests that SUTN9-2 likely evolves resistance mechanisms against CAMPs found in rice, chili, and tomato plants through mechanisms involving the protease-chaperone DegP, AcrAB-TolC multidrug efflux pumps, and polysaccharides. These mechanisms facilitate efflux, degradation, and the formation of protective barriers to resist CAMPs. Such adaptations enable SUTN9-2 to persist and colonize host plants despite antimicrobial pressures, influencing its viability, cell differentiation, and nitrogen fixation during endophytic interactions with various plant hosts.
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spelling doaj-art-69ec589e300143c1822d8e8fcab554402025-01-26T12:29:19ZengNature PortfolioScientific Reports2045-23222025-01-0115112110.1038/s41598-025-87488-5Differential responses of Bradyrhizobium sp. SUTN9-2 to plant extracts and implications for endophytic interactions within different host plantsTeerana Greetatorn0Pakpoom Boonchuen1Pongdet Piromyou2Pongpan Songwattana3Jenjira Wongdee4Kamonluck Teamtisong5Nantakorn Boonkerd6Shusei Sato7Neung Teaumroong8Panlada Tittabutr9Institute of Research and Development, Suranaree University of TechnologySchool of Biotechnology, Institute of Agricultural Technology, Suranaree University of TechnologyInstitute of Research and Development, Suranaree University of TechnologyInstitute of Research and Development, Suranaree University of TechnologyInstitute of Research and Development, Suranaree University of TechnologyCenter for Scientific and Technological Equipment, Suranaree University of TechnologySchool of Biotechnology, Institute of Agricultural Technology, Suranaree University of TechnologyGraduate School of Life Science, Tohoku UniversitySchool of Biotechnology, Institute of Agricultural Technology, Suranaree University of TechnologySchool of Biotechnology, Institute of Agricultural Technology, Suranaree University of TechnologyAbstract Bradyrhizobium sp. strain SUTN9-2 demonstrates cell enlargement, increased DNA content, and efficient nitrogen fixation in response to rice (Oryza sativa) extract. This response is attributed to the interaction between the plant’s cationic antimicrobial peptides (CAMPs) and the Bradyrhizobium BacA-like transporter (BclA), similar to bacteroid in legume nodules. The present study reveals that SUTN9-2 can also establish functional endophytic interactions with chili (Capsicum annuum) and tomato (Solanum lycopersicum) plants. When exposed to extracts from chili and tomato, SUTN9-2 exhibits cell elongation, polyploidy, and reduced cell viability, with the effects being less pronounced for tomato extract. Transcriptomic and cytological analyses revealed that genes associated with CAMP resistance, nitrogen metabolism, nitrogen fixation, defense responses, and secretion systems were upregulated, while genes related to the cell cycle and certain CAMP-resistance mechanisms were downregulated, particularly in response to chili extract. This study suggests that SUTN9-2 likely evolves resistance mechanisms against CAMPs found in rice, chili, and tomato plants through mechanisms involving the protease-chaperone DegP, AcrAB-TolC multidrug efflux pumps, and polysaccharides. These mechanisms facilitate efflux, degradation, and the formation of protective barriers to resist CAMPs. Such adaptations enable SUTN9-2 to persist and colonize host plants despite antimicrobial pressures, influencing its viability, cell differentiation, and nitrogen fixation during endophytic interactions with various plant hosts.https://doi.org/10.1038/s41598-025-87488-5Endophytic interactionsBradyrhizobiumChiliLegume-endophyteCell differentiationNitrogen fixation
spellingShingle Teerana Greetatorn
Pakpoom Boonchuen
Pongdet Piromyou
Pongpan Songwattana
Jenjira Wongdee
Kamonluck Teamtisong
Nantakorn Boonkerd
Shusei Sato
Neung Teaumroong
Panlada Tittabutr
Differential responses of Bradyrhizobium sp. SUTN9-2 to plant extracts and implications for endophytic interactions within different host plants
Scientific Reports
Endophytic interactions
Bradyrhizobium
Chili
Legume-endophyte
Cell differentiation
Nitrogen fixation
title Differential responses of Bradyrhizobium sp. SUTN9-2 to plant extracts and implications for endophytic interactions within different host plants
title_full Differential responses of Bradyrhizobium sp. SUTN9-2 to plant extracts and implications for endophytic interactions within different host plants
title_fullStr Differential responses of Bradyrhizobium sp. SUTN9-2 to plant extracts and implications for endophytic interactions within different host plants
title_full_unstemmed Differential responses of Bradyrhizobium sp. SUTN9-2 to plant extracts and implications for endophytic interactions within different host plants
title_short Differential responses of Bradyrhizobium sp. SUTN9-2 to plant extracts and implications for endophytic interactions within different host plants
title_sort differential responses of bradyrhizobium sp sutn9 2 to plant extracts and implications for endophytic interactions within different host plants
topic Endophytic interactions
Bradyrhizobium
Chili
Legume-endophyte
Cell differentiation
Nitrogen fixation
url https://doi.org/10.1038/s41598-025-87488-5
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